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Submitted 24 May 2015Accepted 18 August 2015Published 10 September 2015
Corresponding authorHelder Gomes Rodrigues,[email protected]
Academic editorLaura Wilson
Additional Information andDeclarations can be found onpage 15
DOI 10.7717/peerj.1233
Copyright2015 Gomes Rodrigues andŠumbera
Distributed underCreative Commons CC-BY 4.0
OPEN ACCESS
Dental peculiarities in the silverymole-rat: an original model for studyingthe evolutionary and biological origins ofcontinuous dental generation inmammalsHelder Gomes Rodrigues1 and Radim Šumbera2
1 Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements (CR2P),UMR CNRS 7207, Museum national d’Histoire naturelle, Université Paris 6, Paris, France
2 Department of Zoology, Faculty of Science, University of South Bohemia, České Budějovice,Czech Republic
ABSTRACTUnravelling the evolutionary and developmental mechanisms that have impacted themammalian dentition, since more than 200 Ma, is an intricate issue. Interestingly, afew mammal species, including the silvery mole-rat Heliophobius argenteocinereus,are able to replace their dentition by the addition of supernumerary molars at theback of jaw migrating then toward the front. The aim here was to demonstrate thepotential interest of further studying this rodent in order to better understand theorigins of continuous dental replacement in mammals, which could also provideinteresting data concerning the evolution of limited dental generation occurring infirst mammals. In the present study, we described the main stages of the dental erup-tive sequence in the silvery mole-rat and the associated characteristics of horizontalreplacement using X-ray microtomography. This was coupled to the investigation ofother African mole-rats which have no dental replacement. This method permittedto establish evidence that the initial development of the dentition in Heliophobius iscomparable to what it is observed in most of African mole-rats. This rodent first haspremolars, but then identical additional molars, a mechanism convergent to man-atees and the pygmy rock-wallaby. Evidence of continuous replacement and strongdental dynamics were also illustrated in Heliophobius, and stressed the need to deeplyinvestigate these aspects for evolutionary, functional and developmental purposes.We also noticed that two groups of extinct non-mammalian synapsids convergentlyacquired this dental mechanism, but in a way differing from extant mammals. Thediscussion on the diverse evolutionary origins of horizontal dental replacement putemphasis on the necessity of focusing on biological parameters potentially involvedin both continuous and limited developments of teeth in mammals. In that context,the silvery mole-rat could appear as the most appropriate candidate to do so.
Subjects Developmental Biology, Evolutionary Studies, ZoologyKeywords Bathyergidae, Teeth, Morphology, Bone remodelling, Replacement, Drift, Resorption,Synapsids
How to cite this article Gomes Rodrigues and Šumbera (2015), Dental peculiarities in the silvery mole-rat: an original model forstudying the evolutionary and biological origins of continuous dental generation in mammals. PeerJ 3:e1233; DOI 10.7717/peerj.1233
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INTRODUCTIONMammals differs from their extinct non-mammalian synapsid relatives by numerous
anatomical, physiological and biological innovations (Kielan-Jaworowska, Cifelli & Luo,
2004; Kemp, 2005). Mammals notably acquired a more complex, but reduced dentition
impacting both number of teeth and number of dental generations (Osborn & Crompton,
1971; Luo, Kielan-Jaworowska & Cifelli, 2004). Numerous studies attempted to study the
biological and functional origins of the reduction of dental replacement in mammals
(e.g., Luckett, 1993; Luo, Kielan-Jaworowska & Cifelli, 2004; Van Nievelt & Smith, 2005).
In that context, the mouse, the traditional biological model, which has however no dental
replacement, has appeared highly valuable to investigate the biological processes involved
in dental development and replacement (e.g., Peterková, Lesot & Peterka, 2006; Jernvall
& Thesleff, 2012; Peterková et al., 2014), also by means of genetically modified specimens
developing supernumerary teeth (e.g., Järvinen et al., 2006; D’Souza & Klein, 2007; Juuri
et al., 2013). Several developmental studies on other mammals, such as minipig, ferret
and mainly humans, provided complementary data on tooth replacement (e.g., Järvinen,
Tummers & Thesleff, 2009; Wang & Fan, 2011; Buchtová et al., 2012).
Continuous dental replacement (CDR) is very rare in mammals. It was first described
in manatees (Trichechus sp.; Stannius, 1845) and in the pygmy rock-wallaby (Petrogale
concinna; Thomas, 1904). This mechanism is described as a continuous development of
teeth at the back of the jaw, then horizontally migrating toward the front, and replacing
anterior cheek teeth shedding (Domning & Hayek, 1984). This kind of horizontal
replacement differs from the continuous replacement of most vertebrates replacing their
teeth locus by locus. The development of additional teeth distally reminds of a mechanism
lost more than 200 Ma ago in first mammals (e.g., Morganucodon†; Luo, Kielan-Jaworowska
& Cifelli, 2004). Consequently, investigating a mammalian model having a continuous
replacement of its dentition would be optimal from evolutionary and developmental
viewpoints. It would allow to compare the mechanisms involved in the continuous
development of teeth in a few extant mammals, with those involved in the regression of
the dental lamina, which prevents dental replacement and additional development of teeth
distally in most mammals (Buchtová et al., 2012). By extension, it would also permit to
better understand what it happened in first mammalian dentition more than 200 Ma ago.
Interestingly, CDR has also recently been described in rodents. It occurs in the silvery
mole-rat, Heliophobius argenteocinereus (Gomes Rodrigues et al., 2011), which is an African
rodent belonging to a strictly subterranean family, the African mole-rats (Bathyergidae).
This species is solitary and occurs in a large area covering Central to Eastern Africa
(Šumbera, Chitaukali & Burda, 2007). It lives in various environments including those
with low food supplies and consisting of seasonally very hard soils, and also in rural areas
where it frequently damages cultivated crops (Šumbera, Chitaukali & Burda, 2007). This
species is not endangered, and could represent a suitable model for studying the origins of
CDR. However, until now, breeding silvery mole-rat in captivity has failed outside of its
area of distribution, probably because of lack of environmental stimuli, which remain to be
discovered.
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The system of CDR is slightly different in this mole-rat inasmuch as teeth are
high-crowned, and the most anterior cheek teeth are totally resorbed inside the bone.
Moreover, if the eruptive dental sequences of manatees and the wallaby are initiated
by the development of premolars (Domning, 1982; Domning & Hayek, 1984; Sanson,
1980; Sanson, 1989), this process is still unknown in the silvery mole-rat, in which
characteristics and dynamics of the dentitions remain to be accurately described. The
silvery mole-rat and especially its relative, the naked mole-rat (Heterocephalus), represent
the oldest bathyergid lineages (Patterson & Upham, 2014). The naked mole-rat lives
in extended families and has a reduced tooth row with only three molars. As most
mole-rats (including fossils) bear one premolar and three molars per tooth row, the most
parsimonious hypothesis would suggest that extinct relatives of Heliophobius had the same
dental formula. However, the functional origin of CDR in Heliophobius remains unclear,
and we wanted to know if the setting up of this mechanism could be related to adaptive
changes from a dentition originally reduced and therefore far less efficient than in other
mole-rats, as supposed in Heterocephalus (Gomes Rodrigues, 2015). This reduced dentition
assumed as a result of relaxed selection could have been associated with cooperative
chisel-tooth digging (Gomes Rodrigues, 2015), whereas the CDR of Heliophobius could have
been selected in relation to a putative higher solitary activity (i.e.; burrowing and foraging),
especially in harder soils, inducing higher dental wear (Gomes Rodrigues et al., 2011).
More generally, the aim of this study is to more accurately describe the morphological
characteristics of the dentition in the silvery mole-rat at different ontogenic stages, and to
compared with other African mole-rats and mammals having CDR. These comparisons
can provide important information on the initiation of the eruptive dental sequence of
Heliophobius, on the putative maintaining of the system during the whole life of the animal,
and on resulting effects on bone tissues. Because teeth are also migrating in the jaw, this
implies bone remodelling in addition to resorption of dental tissues, as for other rodents
showing mesial dental drift, but intensity is expected to vary in relation to the degree of
migration (Gomes Rodrigues et al., 2012; Gomes Rodrigues, 2015). Then, we discussed the
reliability of using this rodent as a future biological model for a better comprehension of
the evolutionary origins of continuous dental generation in mammals and of associated
underlying biological mechanisms.
MATERIAL AND METHODSDental morphologies are difficult to describe in African-mole-rats because their teeth are
rapidly worn and show a flat occlusal surface, which makes difficult putative homologies.
As a result, dentition of very young specimens has been used when available to avoid such
a problem and to draw reliable homologies, as initiated by Denys (1988) who described
juveniles of African mole-rats (i.e.; a specimen of Cryptomys illustrated here, and a spec-
imen of Georychus). Nine specimens of Heliophobius argenteocinereus were investigated
using X-ray synchrotron and conventional microtomography (Table 1). Most individuals
were born in captivity from wild females caught in 2000 and 2005, in Blantyre and Zomba
area located in Southern Malawi. No animals were killed for the purpose of this study; we
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Table 1 Absolute or relative age, and corresponding number of teeth per tooth row for investigated specimens. (x) means presence of not yeterupted tooth.
Family Species Specimen Age Number of cheek teeth
Bathyergidae Heliophobius argenteocinereus ID119 Embryo (1)
ID140 1 day 1(1)
ID142 1 week 1(1)
ID1bis 2 weeks 2
ID2bis 2 months 2(1)
ID13 2 years 4
ID178 4 years 4(1)
ID180 9 years At least 4 andodontoma
RMCA96.036-M-5467 Adult 5(1)
Heterocephalus glaber MNHN-ZM-MO 1884-1578 Adult 3
Bathyergus janetta NHM 47.7.8.26 Juvenile 2
Bathyergus suillus NHM 5.10.8.9 Adult 4
Georychus capensis MNHN-ZM-MO 1988-113 Juvenile 1(1)
NHM 46.11.18.46 Adult 4
Cryptomys hottentotus MNHN-ZM-MO 1988-117 Juvenile 1(1)
Fukomys wandewostijneae NHM 39.291 Adult 4
Macropodidae Petrogale concinna WAM-M8499 Juvenile 4
Trichechidae Trichechus senegalensis M201 Adult 6(1)
only used animals that died naturally. As a result, we did not have access to a complete
ontogenetic series, and dental stages could not be chosen with high precision. Even if no
experiment were conducted on living animals, all manipulations with captive animals were
initially approved by the Control Commission for Ethical Treatment of Animals, University
of South Bohemia, Faculty of Science, Czech Republic (17864/2005-30/300). Scanning of
embryo and juvenile specimens (ID1bis, ID2bis, ID119, ID140, ID142) were realized at
the European Synchrotron Radiation Facility (ESRF, Grenoble, beamline ID 19), with a
pink beam at energy of 60 keV and using a cubic voxel of 7.46 µm. One adult specimen of
Heliophobius (RMCA96.036-M-5467) was also scanned at the ESRF (see Gomes Rodrigues
et al., 2011). Synchrotron microtomography has been proven to be very useful for precise
imaging of small elements, such as teeth (Tafforeau et al., 2006). Other adult specimens
(ID13, ID178, ID180) were scanned using a GE phoenix nanotom 180 at energy of
100 keV with a cubic voxel of 22.73 and 24.29 µm. Non-invasive virtual extractions of
entire dentition (i.e., crown and roots) were realized with VG Studio Max 2.1 software
(VG Studio Max, Heidelberg, Germany). Dentitions of juvenile specimens of other African
mole-rats, such as Cryptomys hottentotus and Georychus capensis housed in the Museum
National d’Histoire Naturelle of Paris (MNHN, France), and Bathyergus janetta housed
in the National History Museum of London (NHM, United Kingdom), were analysed to
draw comparisons (Table 1). Adult specimens of Heterocephalus glaber from the MNHN
of Paris, and Fukomys wandewostijneae, Georychus capensis and Bathyergus suillus from the
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Figure 1 Dental nomenclature used for the Bathyergidae. Dental diagrams of right (A) lower and (B)upper molars of Renefossor songhorensis † (modified from Mein & Pickford, 2008).
NHM of London were also considered (Table 1). Teeth were then described following the
nomenclature of Wood & Wilson (1936) with a few modifications related to Bathyergidae
(Fig. 1). Tx refers to xth upper tooth, Tx to xth lower tooth and Tx to both xth upper and
lower teeth. Alveolar dental walls of specimens of a pygmy rock wallaby from the Western
Australian Museum of Perth (WAM, Australia), and of a manatee from the Poulard’s
collection of the University of Lyon (France) were also investigated (Table 1).
RESULTSOntogenic stages in the silvery mole-ratAn embryo of advanced stage of development shows one mineralized cheek tooth per
dental row (Fig. 2A, ID119), while the second tooth is developing because a bony crypt
can be observed. One day after birth (ID140), the second tooth starts to mineralized. One
week later (ID142), the first tooth starts to erupt, and the second one is more developed but
not yet covered by an enamel layer. A two-week-old specimen shows both teeth erupting
with crown entirely mineralized, but with root still developing (Fig. 2B, ID1bis). After two
months, the first teeth are worn and their root is entirely developed, and the third tooth
is mineralizing and ready to erupt (Fig. 2C, ID2bis). The two-year-old and four-year-old
specimens show the more frequently observed adult dentition, in having four functional
teeth occluding with teeth still erupting distally (Figs. 2D–2E, ID13 and ID178). The first
specimen shows remnants of teeth in resorption (Fig. 2D, ID13), while the mesial most
teeth are highly reduced in the second specimen (Fig. 2E, ID178). The oldest specimen
(nine-year-old) presents an abnormal dentition (Figs. 2F–2H, ID180). Upper and lower
mesial-most teeth are normally developed, but present malocclusions and are ready to
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Figure 2 Dental ontogenic stages in the silvery mole-rat. (A–C) X-ray synchrotron microtomographic 3D rendering of dental rows of juveniles(ID119, ID1bis, ID2bis). (D–E) X-ray conventional microtomographic 3D rendering of dental rows of adult specimens (ID13, ID178). (F–H) X-rayconventional microtomographic 3D rendering of dental rows of the oldest specimen (ID180) showing a bilateral odontoma (dashed line square):(F) right lateral view, (G) anterior view, (F) lateral view showing a virtual section of the left odontoma.
shed, although they are not strongly worn. Moreover, odontomas are formed in the
distal part of the dentition and involved both upper dental rows. These odontomas are
importantly developed, they spread in incisor alveoli, and include numerous malformed
teeth, which subsequently appear in the virtual section (Fig. 2H).
Dental morphology and eruptive sequence in the silvery mole-ratDescriptionCheek teeth of Heliophobius are very high-crowned, but their growth is limited since
their single root is closed at the basal end (Fig. 2). As a result, both upper and lower teeth
are cone-shaped. Unerupted teeth show enamel free areas (i.e., dentine can be already
observed, Fig. 3A). Worn upper teeth shows heart-shaped occlusal surface, while lower
teeth show pear-shaped occlusal surface (Fig. 3C).
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Figure 3 Dental eruptive sequence in the silvery mole-rat compared with other African mole-rats. (A) Comparisons of the morphology of first cheek teeth of juveniles represented by X-ray syn-chrotron microtomographic 3D rendering of a two-week-old silvery mole-rat (ID1bis) and by diagramsfor African mole-rats (Cryptomys hottentotus MNHN-ZM-MO 1988-117, Georychus capensis MNHN-ZM-MO 1988-113, Bathyergus janetta NHM 47.7.8.26). (B) Diagrams of cheek teeth of a 2-month-oldsilvery mole-rat (ID2bis). (C) Diagrams of cheek teeth of a 2-year-old silvery mole-rat (ID13), andadult specimens of African mole-rats, such as Heterocephalus glaber (MNHN-ZM-MO 1884–1578),Fukomys wandewostijneae (NHM 39.291), Georychus capensis (NHM 46.11.18.46), Bathyergus suillus(NHM 5.10.8.9). Not to scale.
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- DP4 of Heliophobius is molariform (Fig. 3A). It shows a mesially located metaconid
compared to the protoconid, which is less developed. The metalophulid I links these
cusps. The metaconid also has a distal spur on the labial border, which reaches the
entoconid and closes the mesosinusid. The ectolophid is marked in its mesial part linked
to the protoconid, but it is interrupted to faintly marked at the level of the hypoconid.
The sinusid is short and transverse. The posterolophid is strong and reaches the distal
part of the entoconid. It can be assumed that the hypolophid transversally joins the
hypoconid and the entoconid because of the crescent shape of the distal dentine area.
- M1 is clearly bilophodont, with an ectolophid missing to reduced, but more centrally
located (Fig. 3A). As a result, the sinusid and the mesosinusid are equal in size.
The mesial lophid consists of the protoconid and the metaconid connected by the
metalophulid I. The distal lophid joins the reduced hypoconid to the entoconid. It is
difficult to state if the hypolophid is present or fused with the posterolophid.
- M2 presents the same pattern, but the second lophid is much more reduced, and shows
reduced entoconid and crest-like hypoconid (Fig. 3B). Following teeth present the same
morphology as well, in having a highly reduced hypoconid (Fig. 3C).
- DP4 is molariform. The protocone is strong and linked to the paracone via the
anteroloph. The paraloph is short and incipient and does not reach the protocone.
Paracone and metacone are contiguous and close the mesosinus. The strong endoloph
joins the protocone and the hypocone, which is mesio-distally compressed. The sinus is
short and transverse. The hypocone is connected to the posteroloph, which distally joins
the metacone. The metaloph is probably absent (Fig. 3A).
- M1 presents a very close pattern (Fig. 3A). However, the paraloph is absent, and the
hypocone is not reduced.
- M2 shows a reduced protocone compared to the paracone (Fig. 3B). The anteroloph is
weak to interrupted between these cusps. The distal part is much more reduced, with a
small hypocone and a highly reduced and crest-like metacone. Following teeth have the
same pattern (Fig. 3C).
Comparisons with other African mole-rats- Heliophobius differs from all bathyergids in having additional molars. These teeth have
highly reduced distal loph and lophids, and are like M3 of African mole-rats (Fig. 3C).
However, it seems inappropriate to draw reliable comparisons between teeth whose
homology is not established even if they are located at the same loci. Heliophobius also
present the highest crown in association with Bathyergus.
- Heliophobius differs from Heterocephalus in having DP4, reduced distal lophid on
M1 and M2 with a weaker ectolophid, more elongated lower molars, and in showing
adjacent paracone and metacone closing the mesosinus in upper molars. Consequently,
Heliophobius presents worn upper teeth with heart-shaped occlusal surface, whereas
Heterocephalus presents worn upper teeth with U-shaped occlusal surface. Some
specimens of Heterocephalus also have highly reduced to missing M3.
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- Heliophobius differs from Cryptomys and Fukomys in having more elongated and less
rounded cheek teeth, but is similar in having a simplified dental pattern with rapidly
poorly distinct loph and lophids due to wear. Heliophobius differs from Cryptomys in
having a metaconid less protruding mesially, a sinusid less protruding distally, and a
hypoconid not reduced on DP4, and in having an ectolophid weaker on lower teeth.
It also has a rounded mesial border without disruption between the paracone and
the metacone on upper teeth, associated with a wider mesosinus because of a shorter
paraloph (probably connected to the endoloph in Cryptomys).
- One of the main differences between Heliophobius and Georychus is about lower teeth.
If the ectolophid is weak in Heliophobius, it is strong and distally connected to the
entoconid in Georychus, and consequently the sinusid is larger and protruding distally.
On DP4, the mesosinusid is closed in Heliophobius, whereas it is open in Georychus.
On upper teeth, Heliophobius differs from Georychus in having a transverse sinus which
is not mesially protruding, in having contiguous paracone and metacone on DP4,
and a more reduced metacone on M2. Heliophobius presents worn upper teeth with
heart-shaped occlusal surface, while Georychus presents worn upper teeth with an
H-shaped occlusal surface.
- Heliophobius differs from Bathyergus in having a metaconid bigger than the protoconid
and slightly protruding mesially, in having uninterrupted ectolophid and hypolophid,
and a posterolophid connected to the entoconid on DP4. If the ectolophid is also weaker
to discontinuous in molars of both genera, this lophid is more centrally located on M1of Heliophobius, in which the hypoconid is more reduced and sinusid and mesosinusid
are more open. Upper teeth of Heliophobius and Bathyergus are morphologically very
close. However, the hypocone is more reduced on the DP4 of Heliophobius, the paraloph
is slightly distinct, and paracone and metacone are closer.
Characteristics of dental resorption and bone remodellingEvidence of continuous mesial drift can be observed in bone tissues for specimens of
a pygmy-rock wallaby, a manatee and a silvery mole-rat (Figs. 4A–4E). In the wallaby,
the interalveolar septum presents a distally compacted aspect resulting from bone
resorption, while the mesial part is illustrated by a high number of openings of vascular
channels due to bone apposition (or formation, Fig. 4A), clearly observed in the manatee
(Fig. 4B). In virtual cross-section of upper cheek teeth in the silvery mole-rat, bone
resorption is shown on mesial side of teeth by the serrated aspect of the distal part of
interalveolar septa, and by the corresponding alveolar wall showing a surface strongly
etched (Figs. 4C–4D). Bone apposition is conversely illustrated on distal side of teeth
by the presence of numerous openings of vascular channels in bone septa and alveolar
surface (Figs. 4C and 4E). In this area, dental resorption also occurs because the enamel
layer is reduced to absent and the outline is irregular due to the indirect compressive
force of erupting distal molars also leading to periodontium disruption. Dental resorption
is strongly efficient at the mesial-most side of the cheek tooth row, where the layer of
cementum tends to be thicker (Fig. 4C).
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Figure 4 Consequences of dental mesial drift on bone tissues in the pygmy rock-wallaby, the manatee,and the silvery mole-rat compared with the felou gundi. (A) Picture of bone remodelling in themandibular alveolar dental wall of a pygmy rock-wallaby (WAM-M8499). Green arrows associated withthe continuous line indicate bone apposition and dashed red arrows associated with the dashed lineindicate bone resorption. See the more compacted bone tissue on the left side and numerous openings ofvascular channels on the left side of the alveolar wall. (B) Picture of bone remodelling in the mandibularalveolar dental wall of a manatee (M201). Blue arrows indicate a few openings of vascular channels. X-raysynchrotron microtomographic study of a specimen of (C–E) a silvery mole-rat (RMCA96.036-M-5467)and of (F–H) a felou gundi (MNHN-ZM-MO 1989-22; modified from Gomes Rodrigues et al., 2012).(C, F) Virtual cross-section of upper dental rows. The white dash line indicates the limit between thecementum layer and the teeth. The large green arrows indicate the direction of dental drift, and theirlength shows the degree of dental migration. (D, G) 3D rendering of the distal part of the alveolar wallshowing an etched surface corresponding to bone resorption (dashed red boxes). (E, H) 3D renderingof the mesial part of the alveolar wall showing openings of vascular channels corresponding to boneapposition (green boxes). Not to scale.
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Figure 5 Phylogeny showing the dental characteristics and dynamics of some synapsids. Simplifieddiagrams of mandible showing the different types of cheek tooth replacement: continuous and alternatevertical replacement (small green arrows in Thrinaxodon†), continuous horizontal replacement (largegreen arrow in Tritylodontidae†), single and sequential vertical replacement (blue arrows in Morganu-codon†). PC, post-canines; dP, deciduous premolars; M, molars. 1. Dental formulae in juveniles. 2. Dentalformulae in adults. P, maximal number of premolars per tooth row; M, maximal number of molars pertooth row. 3. Mode of dental drift. sDD, slight distal drift; sMD, slight mesial drift; mMD, moderatemesial drift; cMD, continuous mesial drift. Blue branch, Muridae; yellow branch, Ctenodactylidae; redbranch, Bathyergidae.
DISCUSSIONNormal initial dental developmentBefore developing supernumerary molars, juveniles of manatees and of the pygmy rock-
wallaby show a dental eruptive sequence similar to other mammals in having deciduous
premolars before molars (Sanson, 1980; Domning, 1982; Gomes Rodrigues et al., 2011;
Fig. 5). One of the major constraints when studying the dentition of the silvery mole-rat
is the very high wear, which does not permit accurate morphological descriptions. The
investigation of very young specimens helps us to determinate the eruptive sequence of
this rodent. As a result, the crown morphology of both first lower and upper erupted
cheek teeth strongly looks like DP4 of other African mole-rats. In DP4 of Heliophobius,
the metaconid is more mesially located as in Cryptomys and Georychus, and the pattern is
more complex than molars, which have a marked bilophodont structure, as in Bathyergus.
The difference between DP4 and lower molars is more subtle, but the paraloph is present
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as in Cryptomys, and the second loph (hypocone-posteroloph-metacone) is not reduced.
This means that the initial development of the cheek tooth row is comparable to what it is
observed in most Bathyergidae, and in mammals with CDR as well (Fig. 5). These results
also corroborate the hypothesis of Landry (1957), who proposed that the fourth premolar
is coupled with molars and “that the extra teeth in Heliophobius represent entirely new
dental elements added on to the end of the usual mammalian series” (p. 68).
Heliophobius has an eruptive dental sequence which differs from Heterocephalus, due
to the occurrence of premolars, as seen in first known bathyergids from the Miocene of
Africa (Mein & Pickford, 2008). Heterocephalus and Heliophobius clearly display derived but
opposite dental evolutionary trends, involving dental reduction in the oldest bathyergid
lineage (only three or two molars, Fig. 5), and development of additional teeth in the
lineage of Heliophobius. Data on extinct relatives of Heliophobius are thus essential to
assess the evolutionary origins and the potential adaptive nature of this mechanism. More
precisely, knowledge of the climatic, environmental and geological contexts relative to the
appearance of CDR is needed. In the meantime, the functional characteristics of CDR
in Heliophobius also remain to be precisely described in vivo, inasmuch as its dentition
including originally four high-crown cheek teeth seems already highly efficient compared
with other mole-rats, having higher bite force at molars, while digging with their incisors
(e.g., Fukomys; Van Daele, Herrel & Adriaens, 2009).
The timing of dental eruptive sequence of Heliophobius is also very close to the timing
known in Georychus, in which a new born has one teeth, a two-week-older specimen
has two erupted teeth, and a four-week specimen has three erupted teeth (Taylor, Jarvis
& Crowe, 1985). Unfortunately, we have no data concerning the development of the
fourth teeth in Heliophobius, which might be tightly associated with the development of
additional molars. It can be only observed that M2 and subsequent molars display a highly
reduced distal parts. The additional molars are very similar to the penultimate molar, as
observed in wallabies, and as noticed by Domning (1982) in manatees: “Trichechids were
turning out unlimited numbers of “second molars” . . . ” (p. 609). More material, as well as
further developmental analyses are needed to precisely describe the formation of supernu-
merary teeth in Heliophobius. More generally, presence of premolars rapidly replaced by
additional molars is another evidence of close convergent dental evolution between very
different mammals, involving a rodent, a sirenian, and a macropod which had to face abra-
sive diet and/or terrigenous matter (Domning, 1982; Sanson, Nelson & Fell, 1985; Gomes
Rodrigues et al., 2011; Škĺıba, Šumbera & Vı́támvás, 2011), probably just after weaning.
Evidence of continuous dental replacementOne of the most interesting point concerns evidence of CDR in Heliophobius. Landry
(1957) proposed that extra teeth can be present in this rodent, while Gomes Rodrigues et
al. (2011) went further and proposed a CDR by analogy with what happens in manatees
and the pygmy rock-wallaby. But, here, the study of the oldest specimen provides another
evidence of continuous generation of teeth. The presence of bilateral odontomas in the
distal part of the dentition in a rodent specimen supposed to have its last molars erupted
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for a while (e.g., between one and two years in Georychus; Taylor, Jarvis & Crowe, 1985)
is intriguing, if we are not aware of the possibility of continuous dental development in
supposed diphyodont animals. But, in the case of mammals with CDR, it can be related to
developmental disruption probably linked to ageing. This was observed in a few specimens
of old mice having bilateral odontomas at the level of the proximal end of incisors, in
relation to their continuous growth (Dayan et al., 1994). This is obviously an evidence
of the maintenance of active dental stem cells at the back of jaw. As incisors were also
involved in this disorder and because their developmental origin is back and very close
to last erupting molars (i.e., in outgrowth of pterygoid processes), a possible molecular
interaction between incisor and molar tissues, which regulates their continuous activity,
cannot be rejected and remains to be investigated. In any event, such results validate the
hypothesis of continuous dental generation in the silvery mole-rat. Only when its breeding
will be possible, precise and detailed investigation of mechanisms of dental development
would permit to test the assumption of an extension of the dental lamina allowing CDR,
conversely to its regression in diphyodont mammals, in which part of developmental
mechanisms have already been described at the histological level (Buchtová et al., 2012).
Evidence of intense dental driftThree stages of dental mesial drift (or physiological drift) were defined in rodents
(Fig. 5). The first one, observed in Georychus and Bathyergus, corresponds to a slight
dental displacement and does not involve any dental loss (Gomes Rodrigues et al.,
2011; Gomes Rodrigues, 2015; Fig. 5). The moderate mesial drift is present in all gundis
(Ctenodactylidae), which only lose anterior teeth under the pressure of erupting posterior
teeth (Gomes Rodrigues et al., 2012; Figs. 4 and 5). The strong or continuous mesial drift
is only known in the silvery mole-rat because of the CDR leading to the constant loss of
teeth at the front of the jaw. This dental dynamic involves bone remodelling and resorption
of dental tissues whose intensity increases according to the degree of dental drift. This is
evidenced when comparing alveolar bone characteristics between gundis (e.g., Felovia,
Figs. 4F–4H; Gomes Rodrigues et al., 2012) and the silvery mole-rat. This latter shows
a higher number of openings of vascular channel when bone is forming, and a more
intensively etched surface when bone is in resorption, as similarly does the pygmy rock
wallaby and the manatee. Moreover, alveolar septa are thinner in Heliophobius compared to
other mole-rats in relation to constant bone remodelling (Gomes Rodrigues, 2015). Mesial
teeth are highly resorbed and constantly covered by a thick layer of cementum, which
might correspond to cementum repair protecting teeth (Jäger et al., 2008), necessary to
maintain anchoring of the teeth in the dental alveolus via the periodontal ligament (Saffar,
Lasfargues & Cherruau, 1997; Fleischmannová et al., 2010). Cemental modifications have
also been reported in manatees (Miller, Sanson & Odell, 1980). The constant formation of
teeth at the back of the jaw drives intense compressive forces which induce strong physical
constraints on the whole dentition and on surrounding tissues (periodontium, alveolar
bone). Nonetheless, dental disorders and misalignments are rare, because of the presence
of a diastema in front of cheek teeth in these mammals.
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The development and functionalization of the tooth in time and space occurred in
close relation with the development of the surrounding bone and periodontal tissues.
Moreover, the homeostasis of the alveolar bone is characterized by a high turn-over
during the life of a tooth and by specific interactions with the periodontal ligament
(Fleischmannová et al., 2010), which are modified during dental drift. The impact of
dental drift has only been studied in the context of orthodontic researches in rat and
mouse (e.g., Ren, Maltha & Kuijpers-Jagtman, 2004; Yoshimatsu et al., 2006), in which the
migration is activated by an experimental system producing tensile forces (Wise & King,
2008). However, rat and mouse were rather described as having a slight distal drift (Johnson
& Martinez, 1998; Fig. 5), without any detail on the cause of migration. The silvery
mole-rat is pertinent for investigating the effect of the permanent migration of teeth on
surrounding tissues involving notably homeostasis of alveolar bone and the periodontium,
and also cementum repairs. The accurate description of the dental dynamics and its impact
on both teeth and bone at the histological level in the silvery mole-rat and in rodents
showing different degrees of drift will permit to comparatively assess the effects of natural
migration and the associated mechanical constraints sustained by the whole masticatory
apparatus. This could provide new insights on the functional properties of these various
masticatory apparatus in relation to the ecology of these rodents.
Evolutionary insights on the horizontal CDRInterestingly, if the silvery mole-rat, manatees, and the pygmy rock-wallaby, represent
unique cases of CDR in mammals, such an extended horizontal replacement has also been
reported in non-mammalian synapsids (i.e., Traversodontidae†: Hopson, 1971; Liu, Bento
Soares & Reichel, 2008; Liu & Sues, 2010; Tritylodontidae†: Kühne, 1956; Cui & Sun, 1987).
These Mesozoic forms were assumed as herbivores and ingested fibrous plants (Kemp,
2005), probably also abrasive. This is more obvious in multi-cuspate tritylodontids (Fig. 5),
especially derived taxa, which have higher dental wear in the mesial part of the dentition,
and show evidence of dental drift and also dental resorption similar to what happen in
manatees (Kühne, 1956; Cui & Sun, 1987; Jasinovski & Chinsamy, 2012).
The central point is that these synapsids acquired an extended or continuous horizontal
replacement of more complex and larger teeth combined with the progressive loss of
anterior post-canines. In addition, this sequential replacement was superimposed to
the initial alternate and vertical replacement known in most non-mammalian synapsids
(e.g., Thrinaxodon†, Fig. 5), which were not limited to two dental generations contrary
to mammals (Hopson, 1971; Osborn & Crompton, 1971). Hopson (1971) partly explained
the reduction of the number of dental generation in mammals, by the presence of more
complex teeth anchored in a socket via periodontal ligaments (i.e., thecodonty) allowing to
cope with mechanical stresses resulting from strong dental pressure during occlusion,
which in contrast makes them more difficult to replace. In that context, eruption of
teeth at the back, drifting then along the jaw, appears as a more suitable means to renew
the dentition, inasmuch that such displacement can be favoured by transseptal fibers
linking adjacent teeth, as noticed by Miller, Sanson & Odell (1980) in manatees, and
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also kangaroos, which have dental drift. However, because of the compressive force of
erupting teeth, the perfect anchoring of teeth is a necessary prerequisite to avoid dental
disorders. Some traversodontids, tritylodontids, manatees, and the pygmy rock-wallaby
have elongated roots, which prevent such problems. The silvery mole-rat is the only
one chisel-tooth digger among bathyergids to have very high-crowned teeth, which are
also cone-shaped as in some traversodontids (e.g., Boreogomphodon†, Liu & Sues, 2010).
That characteristics has probably facilitated the mechanical superimposition of CDR,
whatever its function, as well as mesial drift also observed in other high-crowned mole-rats
(e.g., Bathyergus).
The biological origins of CDR in mammals remains however to discover. Even if
mammals having CDR show striking morphological convergences with non-mammalian
synapsid groups, it seems unlikely that the same developmental pathways permitting
new generation of teeth distally were reactivated after such a very long period of time
(Gomes Rodrigues et al., 2011). Nonetheless, specific biological parameters probably
shared between non-mammalian-synapsids and these mammals might have favoured
the acquisition of CDR. For instance, it should be noticed that these mammals have
low basal metabolic rates (Gallivan & Best, 1980; Janis & Fortelius, 1988; Mc Nab, 2005;
Zelová et al., 2007), as show “reptiles” (i.e., Sauropsida), which generally have continuous
generation of teeth, even if not horizontal. Direct or indirect relations between CDR
and such biological parameters cannot be demonstrated for the moment. In any event,
these troubling “reptile-like” similarities clearly need deeper considerations, and the
silvery mole-rat could appear as an appropriate candidate for further researches. This
will contribute to a better understanding of the origins of the mammalian CDR, but also
to the gathering of new data on the biological mechanisms leading to the reduction of the
dentition at the origin of mammals.
ACKNOWLEDGEMENTSWe are grateful to V Nicolas and C Denys from the MNHN of Paris, to W Wendelen from
the RMCA of Tervuren, to R Portela Miguez from the NHM of London, and to R How
and C Stevenson from the WAM of Perth to allow the visit of mammal collections. We
greatly acknowledge the ESRF (Grenoble), Paul Tafforeau and the team of the beamlines
ID19 to have supported that research project by giving access to their experimental
stations. Thanks to C Charles (Institut de Génomique Fonctionnelle de Lyon, Structure
Fédératrice de Recherche BioSciences UMS3444/US8, Gerland—Lyon Sud) for giving
access to facilities associated with X-ray microtomography. The manuscript benefited from
the constructive comments of two anonymous reviewers, and of the editor.
ADDITIONAL INFORMATION AND DECLARATIONS
FundingThis work benefits from a grant from La Fondation des Treilles (HGR). The funders had no
role in study design, data collection and analysis, decision to publish, or preparation of the
manuscript.
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Grant DisclosuresThe following grant information was disclosed by the authors:
Fondation des Treilles.
Competing InterestsThe authors declare there are no competing interests.
Author Contributions• Helder Gomes Rodrigues conceived and designed the experiments, performed the
experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the
paper, prepared figures and/or tables, reviewed drafts of the paper.
• Radim Šumbera contributed reagents/materials/analysis tools, wrote the paper,
reviewed drafts of the paper.
Animal EthicsThe following information was supplied relating to ethical approvals (i.e., approving body
and any reference numbers):
Even if no experiment were conducted on living animals in this study, all manipulations
with captive animals were initially approved by the Control Commission for Ethical
Treatment of Animals, University of South Bohemia, Faculty of Science, Czech Republic
(17864/2005-30/300).
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Dental peculiarities in the silvery mole-rat: an original model for studying the evolutionary and biological origins of continuous dental generation in mammalsIntroductionMaterial and MethodsResultsOntogenic stages in the silvery mole-ratDental morphology and eruptive sequence in the silvery mole-ratCharacteristics of dental resorption and bone remodelling
DiscussionNormal initial dental developmentEvidence of continuous dental replacementEvidence of intense dental driftEvolutionary insights on the horizontal CDR
AcknowledgementsReferences